A genomic analysis of mouse models of breast cancer reveals molecular features of mouse models and relationships to human breast cancer

Breast Cancer Research

Volumn 16, Issue 3, 2014, Pages

  Hollern, Daniel P ^a   Andrechek, Eran R ^a  

^a MICHIGAN STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CLAUDIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BREAST CANCER; COMPARATIVE STUDY; GENE EXPRESSION; GENE ONTOLOGY; GENETIC HETEROGENEITY; GENOME ANALYSIS; HUMAN; INTRACELLULAR SIGNALING; MOLECULAR GENETICS; MOUSE MAMMARY TUMOR ONCOVIRUS; NONHUMAN; TUMOR GROWTH; UPREGULATION; ANIMAL; BIOLOGY; BREAST TUMOR; CLASSIFICATION; DISEASE MODEL; DNA MICROARRAY; EXPERIMENTAL MAMMARY NEOPLASM; FEMALE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETIC DATABASE; GENETIC VARIABILITY; GENETICS; GENOMICS; MOUSE; ONCOGENE; PATHOLOGY; PROCEDURES; ANIMAL CELL; ANIMAL TISSUE; CANCER GENETICS; CONTROLLED STUDY; GENE IDENTIFICATION; GENETIC ANALYSIS; GENETIC ASSOCIATION; GENETIC TRANSCRIPTION; MICROARRAY ANALYSIS; SIGNAL TRANSDUCTION;

ANIMALS; BREAST NEOPLASMS; COMPUTATIONAL BIOLOGY; DATABASES, GENETIC; DISEASE MODELS, ANIMAL; FEMALE; GENE EXPRESSION; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, NEOPLASTIC; GENETIC VARIATION; GENOMICS; HUMANS; MAMMARY NEOPLASMS, ANIMAL; MAMMARY TUMOR VIRUS, MOUSE; MICE; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; ONCOGENES;

EID: 84901982281     PISSN: 14655411     EISSN: 1465542X     Source Type: Journal    
DOI: 10.1186/bcr3672     Document Type: Article

References (83)

1. Prat A, Parker JS, Karginova O, Fan C, Livasy C, Herschkowitz JI, He X, Perou CM. Phenotypic and molecular characterization of the claudin-low intrinsic subtype of breast cancer. Breast Cancer Res 2010, 12:R68. 10.1186/bcr2635, 3096954, 20813035.
2. Gatza ML, Lucas JE, Barry WT, Kim JW, Wang Q, Crawford MD, Datto MB, Kelley M, Mathey-Prevot B, Potti A, Nevins JR. A pathway-based classification of human breast cancer. Proc Natl Acad Sci U S A 2010, 107:6994-6999. 10.1073/pnas.0912708107, 2872436, 20335537.
3. Callahan R, Smith GH. MMTV-induced mammary tumorigenesis: gene discovery, progression to malignancy and cellular pathways. Oncogene 2000, 19:992-1001. 10.1038/sj.onc.1203276, 10713682.
4. Nusse R, Varmus HE. Many tumors induced by the mouse mammary tumor virus contain a provirus integrated in the same region of the host genome. Cell 1982, 31:99-109. 10.1016/0092-8674(82)90409-3, 6297757.
5. Slamon DJ, Clark GM, Wong SG, Levin WJ, Ullrich A, McGuire WL. Human breast cancer: correlation of relapse and survival with amplification of the HER-2/neu oncogene. Science 1987, 235:177-182. 10.1126/science.3798106, 3798106.
6. Slamon DJ, Godolphin W, Jones LA, Holt JA, Wong SG, Keith DE, Levin WJ, Stuart SG, Udove J, Ullrich A, Press MF. Studies of the HER-2/neu proto-oncogene in human breast and ovarian cancer. Science 1989, 244:707-712. 10.1126/science.2470152, 2470152.
7. Muller WJ, Sinn E, Pattengale PK, Wallace R, Leder P. Single-step induction of mammary adenocarcinoma in transgenic mice bearing the activated c-neu oncogene. Cell 1988, 54:105-115. 10.1016/0092-8674(88)90184-5, 2898299.
8. Andrechek ER, Hardy WR, Siegel PM, Rudnicki MA, Cardiff RD, Muller WJ. Amplification of the neu/erbB-2 oncogene in a mouse model of mammary tumorigenesis. Proc Natl Acad Sci U S A 2000, 97:3444-3449. 10.1073/pnas.97.7.3444, 16259, 10716706.
9. D'Cruz CM, Gunther EJ, Boxer RB, Hartman JL, Sintasath L, Moody SE, Cox JD, Ha SI, Belka GK, Golant A, Cardiff RD, Chodosh LA. c-MYC induces mammary tumorigenesis by means of a preferred pathway involving spontaneous Kras2 mutations. Nat Med 2001, 7:235-239. 10.1038/84691, 11175856.
10. Fluck MM, Schaffhausen BS. Lessons in signaling and tumorigenesis from polyomavirus middle T antigen. Microbiol Mol Biol Rev 2009, 73:542-563. Table of Contents, 10.1128/MMBR.00009-09, 2738132, 19721090.
11. Herschkowitz JI, Zhao W, Zhang M, Usary J, Murrow G, Edwards D, Knezevic J, Greene SB, Darr D, Troester MA, Hilsenbeck SG, Medina D, Perou CM, Rosen JM. Comparative oncogenomics identifies breast tumors enriched in functional tumor-initiating cells. Proc Natl Acad Sci U S A 2011, 109:2778-2783. 3286979, 21633010.
12. Hunter KW, Broman KW, Voyer TL, Lukes L, Cozma D, Debies MT, Rouse J, Welch DR. Predisposition to efficient mammary tumor metastatic progression is linked to the breast cancer metastasis suppressor gene Brms1. Cancer Res 2001, 61:8866-8872.
13. Andrechek ER, Laing MA, Girgis-Gabardo AA, Siegel PM, Cardiff RD, Muller WJ. Gene expression profiling of neu-induced mammary tumors from transgenic mice reveals genetic and morphological similarities to ErbB2-expressing human breast cancers. Cancer Res 2003, 63:4920-4926.
14. Rosner A, Miyoshi K, Landesman-Bollag E, Xu X, Seldin DC, Moser AR, MacLeod CL, Shyamala G, Gillgrass AE, Cardiff RD. Pathway pathology: histological differences between ErbB/Ras and Wnt pathway transgenic mammary tumors. Am J Pathol 2002, 161:1087-1097. 10.1016/S0002-9440(10)64269-1, 1867237, 12213737.
15. Andrechek ER, Cardiff RD, Chang JT, Gatza ML, Acharya CR, Potti A, Nevins JR. Genetic heterogeneity of Myc-induced mammary tumors reflecting diverse phenotypes including metastatic potential. Proc Natl Acad Sci U S A 2009, 106:16387-16392. 10.1073/pnas.0901250106, 2752567, 19805309.
16. Ponzo MG, Lesurf R, Petkiewicz S, O'Malley FP, Pinnaduwage D, Andrulis IL, Bull SB, Chughtai N, Zuo D, Souleimanova M, Germain D, Omeroglu A, Cardiff RD, Hallett M, Park M. Met induces mammary tumors with diverse histologies and is associated with poor outcome and human basal breast cancer. Proc Natl Acad Sci U S A 2009, 106:12903-12908. 10.1073/pnas.0810402106, 2722321, 19617568.
17. Knight JF, Lesurf R, Zhao H, Pinnaduwage D, Davis RR, Saleh SM, Zuo D, Naujokas MA, Chughtai N, Herschkowitz JI, Prat A, Mulligan AM, Muller WJ, Cardiff RD, Gregg JP, Andrulis IL, Hallett MT, Park M. Met synergizes with p53 loss to induce mammary tumors that possess features of claudin-low breast cancer. Proc Natl Acad Sci U S A 2013, 110:E1301-E1310. 10.1073/pnas.1210353110, 3619286, 23509284.
18. Herschkowitz JI, Simin K, Weigman VJ, Mikaelian I, Usary J, Hu Z, Rasmussen KE, Jones LP, Assefnia S, Chandrasekharan S, Backlund MG, Yin Y, Khramtsov AI, Bastein R, Quackenbush J, Glazer RI, Brown PH, Green JE, Kopelovich L, Furth PA, Palazzo JP, Olopade OI, Bernard PS, Churchill GA, Van Dyke T, Perou CM. Identification of conserved gene expression features between murine mammary carcinoma models and human breast tumors. Genome Biol 2007, 8:R76. 10.1186/gb-2007-8-5-r76, 1929138, 17493263.
19. Hollern DP, Yuwanita I, Andrechek ER. A mouse model with T58A mutations in Myc reduces the dependence on KRas mutations and has similarities to claudin-low human breast cancer. Oncogene 2012, 32:1296-1304.
20. Fujiwara K, Yuwanita I, Hollern DP, Andrechek ER. Prediction and genetic demonstration of a role for activator E2Fs in myc-induced tumors. Cancer Res 2011, 71:1924-1932. 10.1158/0008-5472.CAN-10-2386, 21245101.
21. Schade B, Lesurf R, Sanguin-Gendreau V, Bui T, Deblois G, O'Toole SA, Millar EK, Zardawi SJ, Lopez-Knowles E, Sutherland RL, Giguère V, Kahn M, Hallett M, Muller WJ. beta-catenin signaling is a critical event in ErbB2-mediated mammary tumor progression. Cancer Res 2013, 73:4474-4487. 10.1158/0008-5472.CAN-12-3925, 23720052.
22. Dourdin N, Schade B, Lesurf R, Hallett M, Munn RJ, Cardiff RD, Muller WJ. Phosphatase and tensin homologue deleted on chromosome 10 deficiency accelerates tumor induction in a mouse model of ErbB-2 mammary tumorigenesis. Cancer Res 2008, 68:2122-2131. 10.1158/0008-5472.CAN-07-5727, 2752841, 18381417.
23. Carvalho CM, Chang J, Lucas JE, Nevins JR, Wang Q, West M. High-dimensional sparse factor modeling: applications in gene expression genomics. J Am Stat Assoc 2008, 103:1438-1456. 10.1198/016214508000000869, 3017385, 21218139.
24. http://www.stat.duke.edu/research/software/west/bfrm/download.html.
25. http://chipcomparer.genome.duke.edu/.
26. http://filemerger.genome.duke.edu/.
27. Johnson WE, Li C, Rabinovic A. Adjusting batch effects in microarray expression data using empirical Bayes methods. Biostatistics 2007, 8:118-127. 10.1093/biostatistics/kxj037, 16632515.
28. http://www.bu.edu/jlab/wp-assets/ComBat/Download.html.
29. Tusher VG, Tibshirani R, Chu G. Significance analysis of microarrays applied to the ionizing radiation response. Proc Natl Acad Sci U S A 2001, 98:5116-5121. 10.1073/pnas.091062498, 33173, 11309499.
30. http://gather.genome.duke.edu/.
31. http://genepattern.broadinstitute.org/gp/pages/login.jsf.
32. Lim E, Wu D, Pal B, Bouras T, Asselin-Labat ML, Vaillant F, Yagita H, Lindeman GJ, Smyth GK, Visvader JE. Transcriptome analyses of mouse and human mammary cell subpopulations reveal multiple conserved genes and pathways. Breast Cancer Res 2010, 12:R21. 10.1186/bcr2560, 2879567, 20346151.
33. Bild AH, Yao G, Chang JT, Wang Q, Potti A, Chasse D, Joshi MB, Harpole D, Lancaster JM, Berchuck A, Olson JA, Marks JR, Dressman HK, West M, Nevins JR. Oncogenic pathway signatures in human cancers as a guide to targeted therapies. Nature 2006, 439:353-357. 10.1038/nature04296, 16273092.
34. https://genepattern.genome.duke.edu/gp/pages/login.jsf.
35. Wertheim GB, Yang TW, Pan TC, Ramne A, Liu Z, Gardner HP, Dugan KD, Kristel P, Kreike B, van de Vijver MJ, Cardiff RD, Reynolds C, Chodosh LA. The Snf1-related kinase, Hunk, is essential for mammary tumor metastasis. Proc Natl Acad Sci U S A 2009, 106:15855-15860. 10.1073/pnas.0906993106, 2734880, 19717424.
36. Sandgren EP, Schroeder JA, Qui TH, Palmiter RD, Brinster RL, Lee DC. Inhibition of mammary gland involution is associated with transforming growth factor alpha but not c-myc-induced tumorigenesis in transgenic mice. Cancer Res 1995, 55:3915-3927.
37. Leung JY, Andrechek ER, Cardiff RD, Nevins JR. Heterogeneity in MYC-induced mammary tumors contributes to escape from oncogene dependence. Oncogene 2012, 31:2545-2554. 10.1038/onc.2011.433, 3356601, 21996730.
38. Zhu M, Yi M, Kim CH, Deng C, Li Y, Medina D, Stephens RM, Green JE. Integrated miRNA and mRNA expression profiling of mouse mammary tumor models identifies miRNA signatures associated with mammary tumor lineage. Genome Biol 2011, 12:R77. 10.1186/gb-2011-12-8-r77, 3245617, 21846369.
39. Ranger JJ, Levy DE, Shahalizadeh S, Hallett M, Muller WJ. Identification of a Stat3-dependent transcription regulatory network involved in metastatic progression. Cancer Res 2009, 69:6823-6830. 10.1158/0008-5472.CAN-09-1684, 2841985, 19690134.
40. Guy CT, Webster MA, Schaller M, Parsons TJ, Cardiff RD, Muller WJ. Expression of the neu protooncogene in the mammary epithelium of transgenic mice induces metastatic disease. Proc Natl Acad Sci U S A 1992, 89:10578-10582. 10.1073/pnas.89.22.10578, 50384, 1359541.
41. Schade B, Rao T, Dourdin N, Lesurf R, Hallett M, Cardiff RD, Muller WJ. PTEN deficiency in a luminal ErbB-2 mouse model results in dramatic acceleration of mammary tumorigenesis and metastasis. J Biol Chem 2009, 284:19018-19026. 10.1074/jbc.M109.018937, 2707232, 19435886.
42. Schade B, Lam SH, Cernea D, Sanguin-Gendreau V, Cardiff RD, Jung BL, Hallett M, Muller WJ. Distinct ErbB-2 coupled signaling pathways promote mammary tumors with unique pathologic and transcriptional profiles. Cancer Res 2007, 67:7579-7588. 10.1158/0008-5472.CAN-06-4724, 17699761.
43. Ursini-Siegel J, Cory S, Zuo D, Hardy WR, Rexhepaj E, Lam S, Schade B, Jirstrom K, Bjur E, Piccirillo CA, Denardo D, Coussens LM, Brennan DJ, Gallagher WM, Park M, Pawson T, Hallett M, Muller WJ. Receptor tyrosine kinase signaling favors a protumorigenic state in breast cancer cells by inhibiting the adaptive immune response. Cancer Res 2010, 70:7776-7787. 10.1158/0008-5472.CAN-10-2229, 3660232, 20924104.
44. Schoenherr RM, Kelly-Spratt KS, Lin C, Whiteaker JR, Liu T, Holzman T, Coleman I, Feng LC, Lorentzen TD, Krasnoselsky AL, Wang P, Liu Y, Gurley KE, Amon LM, Schepmoes AA, Moore RJ, Camp DG, Chodosh LA, Smith RD, Nelson PS, McIntosh MW, Kemp CJ, Paulovich AG. Proteome and transcriptome profiles of a Her2/Neu-driven mouse model of breast cancer. Proteomics Clin Appl 2011, 5:179-188. 10.1002/prca.201000037, 3069718, 21448875.
45. Guy CT, Cardiff RD, Muller WJ. Induction of mammary tumors by expression of polyomavirus middle T oncogene: a transgenic mouse model for metastatic disease. Mol Cell Biol 1992, 12:954-961. 369527, 1312220.
46. Hu Y, Wu G, Rusch M, Lukes L, Buetow KH, Zhang J, Hunter KW. Integrated cross-species transcriptional network analysis of metastatic susceptibility. Proc Natl Acad Sci U S A 2012, 109:3184-3189. 10.1073/pnas.1117872109, 3286991, 22308418.
47. Bu W, Chen J, Morrison GD, Huang S, Creighton CJ, Huang J, Chamness GC, Hilsenbeck SG, Roop DR, Leavitt AD, Li Y. Keratin 6a marks mammary bipotential progenitor cells that can give rise to a unique tumor model resembling human normal-like breast cancer. Oncogene 2011, 30:4399-4409. 10.1038/onc.2011.147, 3156856, 21532625.
48. Flowers M, Schroeder JA, Borowsky AD, Besselsen DG, Thomson CA, Pandey R, Thompson PA. Pilot study on the effects of dietary conjugated linoleic acid on tumorigenesis and gene expression in PyMT transgenic mice. Carcinogenesis 2010, 31:1642-1649. 10.1093/carcin/bgq148, 2930807, 20624750.
49. Klein A, Wessel R, Graessmann M, Jurgens M, Petersen I, Schmutzler R, Niederacher D, Arnold N, Meindl A, Scherneck S, Seitz S, Graessmann A. Comparison of gene expression data from human and mouse breast cancers: identification of a conserved breast tumor gene set. Int J Cancer 2007, 121:683-688. 10.1002/ijc.22630, 17410534.
50. Maroulakou IG, Anver M, Garrett L, Green JE. Prostate and mammary adenocarcinoma in transgenic mice carrying a rat C3(1) simian virus 40 large tumor antigen fusion gene. Proc Natl Acad Sci U S A 1994, 91:11236-11240. 10.1073/pnas.91.23.11236, 45202, 7972041.
51. Kretschmer C, Sterner-Kock A, Siedentopf F, Schoenegg W, Schlag PM, Kemmner W. Identification of early molecular markers for breast cancer. Mol Cancer 2011, 10:15. 10.1186/1476-4598-10-15, 3045364, 21314937.
52. Zhang M, Behbod F, Atkinson RL, Landis MD, Kittrell F, Edwards D, Medina D, Tsimelzon A, Hilsenbeck S, Green JE, Michalowska AM, Rosen JM. Identification of tumor-initiating cells in a p53-null mouse model of breast cancer. Cancer Res 2008, 68:4674-4682. 10.1158/0008-5472.CAN-07-6353, 2459340, 18559513.
53. Backlund MG, Trasti SL, Backlund DC, Cressman VL, Godfrey V, Koller BH. Impact of ionizing radiation and genetic background on mammary tumorigenesis in p53-deficient mice. Cancer Res 2001, 61:6577-6582.
54. Li Z, Tognon CE, Godinho FJ, Yasaitis L, Hock H, Herschkowitz JI, Lannon CL, Cho E, Kim SJ, Bronson RT, Perou CM, Sorensen PH, Orkin SH. ETV6-NTRK3 fusion oncogene initiates breast cancer from committed mammary progenitors via activation of AP1 complex. Cancer Cell 2007, 12:542-558. 10.1016/j.ccr.2007.11.012, 2175032, 18068631.
55. Xu X, Wagner KU, Larson D, Weaver Z, Li C, Ried T, Hennighausen L, Wynshaw-Boris A, Deng CX. Conditional mutation of Brca1 in mammary epithelial cells results in blunted ductal morphogenesis and tumour formation. Nat Genet 1999, 22:37-43. 10.1038/8743, 10319859.
56. Cho RW, Wang X, Diehn M, Shedden K, Chen GY, Sherlock G, Gurney A, Lewicki J, Clarke MF. Isolation and molecular characterization of cancer stem cells in MMTV-Wnt-1 murine breast tumors. Stem Cells 2008, 26:364-371. 10.1634/stemcells.2007-0440, 17975224.
57. Tsukamoto AS, Grosschedl R, Guzman RC, Parslow T, Varmus HE. Expression of the int-1 gene in transgenic mice is associated with mammary gland hyperplasia and adenocarcinomas in male and female mice. Cell 1988, 55:619-625. 10.1016/0092-8674(88)90220-6, 3180222.
58. Pond AC, Herschkowitz JI, Schwertfeger KL, Welm B, Zhang Y, York B, Cardiff RD, Hilsenbeck S, Perou CM, Creighton CJ, Lloyd RE, Rosen JM. Fibroblast growth factor receptor signaling dramatically accelerates tumorigenesis and enhances oncoprotein translation in the mouse mammary tumor virus-Wnt-1 mouse model of breast cancer. Cancer Res 2010, 70:4868-4879. 10.1158/0008-5472.CAN-09-4404, 3005245, 20501844.
59. Franks SE, Campbell CI, Barnett EF, Siwicky MD, Livingstone J, Cory S, Moorehead RA. Transgenic IGF-IR overexpression induces mammary tumors with basal-like characteristics, whereas IGF-IR-independent mammary tumors express a claudin-low gene signature. Oncogene 2011, 31:3298-3309. 3391665, 22020329.
60. Liu S, Umezu-Goto M, Murph M, Lu Y, Liu W, Zhang F, Yu S, Stephens LC, Cui X, Murrow G, Coombes K, Muller W, Hung MC, Perou CM, Lee AV, Fang X, Mills GB. Expression of autotaxin and lysophosphatidic acid receptors increases mammary tumorigenesis, invasion, and metastases. Cancer Cell 2009, 15:539-550. 10.1016/j.ccr.2009.03.027, 19477432.
61. Bultman SJ, Herschkowitz JI, Godfrey V, Gebuhr TC, Yaniv M, Perou CM, Magnuson T. Characterization of mammary tumors from Brg1 heterozygous mice. Oncogene 2008, 27:460-468. 10.1038/sj.onc.1210664, 17637742.
62. Yin Y, Bai R, Russell RG, Beildeck ME, Xie Z, Kopelovich L, Glazer RI. Characterization of medroxyprogesterone and DMBA-induced multilineage mammary tumors by gene expression profiling. Mol Carcinog 2005, 44:42-50. 10.1002/mc.20119, 15937957.
63. Gallahan D, Jhappan C, Robinson G, Hennighausen L, Sharp R, Kordon E, Callahan R, Merlino G, Smith GH. Expression of a truncated Int3 gene in developing secretory mammary epithelium specifically retards lobular differentiation resulting in tumorigenesis. Cancer Res 1996, 56:1775-1785.
64. Jiang Z, Deng T, Jones R, Li H, Herschkowitz JI, Liu JC, Weigman VJ, Tsao MS, Lane TF, Perou CM, Zacksenhaus E. Rb deletion in mouse mammary progenitors induces luminal-B or basal-like/EMT tumor subtypes depending on p53 status. J Clin Invest 2010, 120:3296-3309. 10.1172/JCI41490, 2929714, 20679727.
65. Kuraguchi M, Ohene-Baah NY, Sonkin D, Bronson RT, Kucherlapati R. Genetic mechanisms in Apc-mediated mammary tumorigenesis. PLoS Genet 2009, 5:e1000367. 10.1371/journal.pgen.1000367, 2629572, 19197353.
66. Chan SR, Vermi W, Luo J, Lucini L, Rickert C, Fowler AM, Lonardi S, Arthur C, Young LJ, Levy DE, Welch MJ, Cardiff RD, Schreiber RD. STAT1-deficient mice spontaneously develop estrogen receptor alpha-positive luminal mammary carcinomas. Breast Cancer Res 2012, 14:R16. 10.1186/bcr3100, 3496133, 22264274.
67. Pollock CB, Yin Y, Yuan H, Zeng X, King S, Li X, Kopelovich L, Albanese C, Glazer RI. PPARdelta activation acts cooperatively with 3-phosphoinositide-dependent protein kinase-1 to enhance mammary tumorigenesis. PLoS One 2011, 6:e16215. 10.1371/journal.pone.0016215, 3020974, 21297860.
68. McCarthy A, Savage K, Gabriel A, Naceur C, Reis-Filho JS, Ashworth A. A mouse model of basal-like breast carcinoma with metaplastic elements. J Pathol 2007, 211:389-398. 10.1002/path.2124, 17212342.
69. Kumar R, Medina D, Sukumar S. Activation of H-ras oncogenes in preneoplastic mouse mammary tissues. Oncogene 1990, 5:1271-1277.
70. Kim S, Roopra A, Alexander CM. A phenotypic mouse model of basaloid breast tumors. PLoS One 2012, 7:e30979. 10.1371/journal.pone.0030979, 3276569, 22347416.
71. Jin W, Yun C, Hobbie A, Martin MJ, Sorensen PH, Kim SJ. Cellular transformation and activation of the phosphoinositide-3-kinase-Akt cascade by the ETV6-NTRK3 chimeric tyrosine kinase requires c-Src. Cancer Res 2007, 67:3192-3200. 10.1158/0008-5472.CAN-06-3526, 17409427.
72. Maroulakou IG, Oemler W, Naber SP, Tsichlis PN. Akt1 ablation inhibits, whereas Akt2 ablation accelerates, the development of mammary adenocarcinomas in mouse mammary tumor virus (MMTV)-ErbB2/neu and MMTV-polyoma middle T transgenic mice. Cancer Res 2007, 67:167-177. 10.1158/0008-5472.CAN-06-3782, 17210696.
73. Khalil S, Tan GA, Giri DD, Zhou XK, Howe LR. Activation status of Wnt/ss-catenin signaling in normal and neoplastic breast tissues: relationship to HER2/neu expression in human and mouse. PLoS One 2012, 7:e33421. 10.1371/journal.pone.0033421, 3311643, 22457761.
74. Wang J, Fu L, Gu F, Ma Y. Notch1 is involved in migration and invasion of human breast cancer cells. Oncol Rep 2011, 26:1295-1303.
75. Muraoka RS, Dumont N, Ritter CA, Dugger TC, Brantley DM, Chen J, Easterly E, Roebuck LR, Ryan S, Gotwals PJ, Koteliansky V, Arteaga CL. Blockade of TGF-beta inhibits mammary tumor cell viability, migration, and metastases. J Clin Invest 2002, 109:1551-1559. 10.1172/JCI0215234, 151012, 12070302.
76. Guy CT, Muthuswamy SK, Cardiff RD, Soriano P, Muller WJ. Activation of the c-Src tyrosine kinase is required for the induction of mammary tumors in transgenic mice. Genes Dev 1994, 8:23-32. 10.1101/gad.8.1.23, 7507074.
77. Liu ML, Von Lintig FC, Liyanage M, Shibata MA, Jorcyk CL, Ried T, Boss GR, Green JE. Amplification of Ki-ras and elevation of MAP kinase activity during mammary tumor progression in C3(1)/SV40 Tag transgenic mice. Oncogene 1998, 17:2403-2411. 10.1038/sj.onc.1202456, 9811472.
78. Taneja P, Zhu S, Maglic D, Fry EA, Kendig RD, Inoue K. Transgenic and knockout mice models to reveal the functions of tumor suppressor genes. Clin Med Insights Oncol 2011, 5:235-257. 3153120, 21836819.
79. Jackson JG, Pant V, Li Q, Chang LL, Quintas-Cardama A, Garza D, Tavana O, Yang P, Manshouri T, Li Y, El-Naggar AK, Lozano G. p53-mediated senescence impairs the apoptotic response to chemotherapy and clinical outcome in breast cancer. Cancer Cell 2012, 21:793-806. 10.1016/j.ccr.2012.04.027, 3376352, 22698404.
80. Perou CM, Jeffrey SS, van de Rijn M, Rees CA, Eisen MB, Ross DT, Pergamenschikov A, Williams CF, Zhu SX, Lee JC, Lashkari D, Shalon D, Brown PO, Botstein D. Distinctive gene expression patterns in human mammary epithelial cells and breast cancers. Proc Natl Acad Sci U S A 1999, 96:9212-9217. 10.1073/pnas.96.16.9212, 17759, 10430922.
81. Cardiff RD, Anver MR, Gusterson BA, Hennighausen L, Jensen RA, Merino MJ, Rehm S, Russo J, Tavassoli FA, Wakefield LM, Ward JM, Green JE. The mammary pathology of genetically engineered mice: the consensus report and recommendations from the Annapolis meeting. Oncogene 2000, 19:968-988. 10.1038/sj.onc.1203277, 10713680.
82. Dillon RL, Brown ST, Ling C, Shioda T, Muller WJ. An EGR2/CITED1 transcription factor complex and the 14-3-3sigma tumor suppressor are involved in regulating ErbB2 expression in a transgenic-mouse model of human breast cancer. Mol Cell Biol 2007, 27:8648-8657. 10.1128/MCB.00866-07, 2169423, 17938205.
83. DeRose YS, Wang G, Lin YC, Bernard PS, Buys SS, Ebbert MT, Factor R, Matsen C, Milash BA, Nelson E, Neumayer L, Randall RL, Stijleman IJ, Welm BE, Welm AL. Tumor grafts derived from women with breast cancer authentically reflect tumor pathology, growth, metastasis and disease outcomes. Nat Med 2011, 17:1514-1520. 10.1038/nm.2454, 3553601, 22019887.